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Abstract Insects often harbour heritable symbionts that provide defence against specialized natural enemies, yet little is known about symbiont protection when hosts face simultaneous threats. In pea aphids (Acyrthosiphon pisum), the facultative endosymbiontHamiltonella defensaconfers protection against the parasitoid,Aphidius ervi, andRegiella insecticolaprotects against aphid‐specific fungal pathogens, includingPandora neoaphidis. Here, we investigated whether these two common aphid symbionts protect against a specialized virusA. pisum virus(APV), and whether their antifungal and antiparasitoid services are impacted by APV infection. We found that APV imposed large fitness costs on symbiont‐free aphids and these costs were elevated in aphids also housingH. defensa. In contrast, APV titres were significantly reduced and costs to APV infection were largely eliminated in aphids withR. insecticola. To our knowledge,R. insecticolais the first aphid symbiont shown to protect against a viral pathogen, and only the second arthropod symbiont reported to do so. In contrast, APV infection did not impact the protective services of eitherR. insecticolaorH. defensa. To better understand APV biology, we produced five genomes and examined transmission routes. We found that moderate rates of vertical transmission, combined with horizontal transfer through food plants, were the major route of APV spread, although lateral transfer by parasitoids also occurred. Transmission was unaffected by facultative symbionts. In summary, the presence and species identity of facultative symbionts resulted in highly divergent outcomes for aphids infected with APV, while not impacting defensive services that target other enemies. These findings add to the diverse phenotypes conferred by aphid symbionts, and to the growing body of work highlighting extensive variation in symbiont‐mediated interactions.
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Warmer nights offer no respite for a defensive mutualism
Abstract Ecologically relevant symbioses are widespread in terrestrial arthropods but based on recent findings these specialized interactions are likely to be especially vulnerable to climate warming. Importantly, empirical data and climate models indicate that warming is occurring asynchronously, with night‐time temperatures increasing faster than daytime temperatures. Daytime (DTW) and night‐time warming (NTW) may impact ectothermic animals and their interactions differently as DTW results in greater daily temperature variation and moves organisms nearer to their thermal limits, while NTW avoids thermal limits and may relieve constraints of cooler night‐time temperatures; a nuance that has largely been ignored in the literature.In laboratory experiments, we investigated how the timing of warming influences a widespread defensive mutualism involving the pea aphidAcyrthosiphon pisum, and its heritable symbiont,Hamiltonella defensa, which protects against an important natural enemy, the parasitic waspAphidius ervi.Three aphid sublines were experimentally created from single aphid genotype susceptible toA. ervi: one line infected with a highly protectiveH. defensastrain, one infected with a moderately protective strain and one without any facultative symbiont. We examined aphid fitness in the presence and absence of parasitoids and when exposed to an average 2.5°C increase occurring across three warming scenarios (night‐time vs. daytime vs. uniform) relative to no‐warming controls.An increase of 2.5°C, as predicted to occur by the IPCC before 2100, was sufficient to disable the aphid defensive mutualism regardless of the timing of warming; a surprising result given that the daily maxima for control and NTW scenarios were identical. We also found that warming negatively impacted (a) symbiont‐mediated interactions between host and parasitoid more than symbiont‐free ones; (b) species interactions (host–parasitoid) more than each participant independently and (c) aphids more than parasitoids even though higher trophic levels are generally predicted to be more affected by warming.Here we show that 2.5°C warming, regardless of timing, negatively impacted a common microbe‐mediated defensive mutualism. While this was a laboratory‐based study, results suggest that temperature increases predicted in the near‐term may disrupt the many ecological symbioses present in terrestrial ecosystems.
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- Award ID(s):
- 1754302
- PAR ID:
- 10456845
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Journal of Animal Ecology
- Volume:
- 89
- Issue:
- 8
- ISSN:
- 0021-8790
- Page Range / eLocation ID:
- p. 1895-1905
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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